相关论文

Global Proteome Analyses of Lysine Acetylation and Succinylation Reveal the Widespread Involvement of both Modification in Metabolism in the Embryo of Germinating Rice Seed.

Abstract:Regulation of rice seed germination has been shown to mainly occur at post-transcriptional levels, of which the changes on proteome status is a major one. Lysine acetylation and succinylation are two prevalent protein post-translational modifications (PTMs) involved in multiple biological processes, especially for metabolism regulation. To investigate the potential mechanism controlling metabolism regulation in rice seed germination, we performed the lysine acetylation and succinylation analyses simultaneously. Using high-accuracy nano-LC-MS/MS in combination with the enrichment of lysine acetylated or succinylated peptides from digested embryonic proteins of 24 h after imbibition (HAI) rice seed, a total of 699 acetylated sites from 389 proteins and 665 succinylated sites from 261 proteins were identified. Among these modified lysine sites, 133 sites on 78 proteins were commonly modified by two PTMs. The overlapped PTM sites were more likely to be in polar acidic/basic amino acid regions and exposed on the protein surface. Both of the acetylated and succinylated proteins cover nearly all aspects of cellular functions. Ribosome complex and glycolysis/gluconeogenesis-related proteins were significantly enriched in both acetylated and succinylated protein profiles through KEGG enrichment and protein-protein interaction network analyses. The acetyl-CoA and succinyl-CoA metabolism-related enzymes were found to be extensively modified by both modifications, implying the functional interaction between the two PTMs. This study provides a rich resource to examine the modulation of the two PTMs on the metabolism pathway and other biological processes in germinating rice seed.

参考文献

[1]  Z. Chen,et al.  Roles of dynamic and reversible histone acetylation in plant development and polyploidy. , 2007, Biochimica et biophysica acta.

[2]  R. Schneider,et al.  Dynamics and interplay of nuclear architecture, genome organization, and gene expression. , 2007, Genes & development.

[3]  I. Finkemeier,et al.  Mitochondrial energy and redox signaling in plants. , 2013, Antioxidants & redox signaling.

[4]  C. Olsen,et al.  Expansion of the lysine acylation landscape. , 2012, Angewandte Chemie.

[5]  F. Ge,et al.  Acetylome Analysis Reveals Diverse Functions of Lysine Acetylation in Mycobacterium tuberculosis* , 2014, Molecular & Cellular Proteomics.

[6]  F. Tan,et al.  Global Analysis of Lysine Acetylation Suggests the Involvement of Protein Acetylation in Diverse Biological Processes in Rice (Oryza sativa) , 2014, PloS one.

[7]  L. Sweetlove,et al.  ROS signalling--specificity is required. , 2010, Trends in plant science.

[8]  Johan Auwerx,et al.  Sirt5 Is a NAD-Dependent Protein Lysine Demalonylase and Desuccinylase , 2011, Science.

[9]  Yu Xue,et al.  CPLA 1.0: an integrated database of protein lysine acetylation , 2010, Nucleic Acids Res..

[10]  Daoxiu Zhou,et al.  Histone acetyltransferase AtGCN5/HAG1 is a versatile regulator of developmental and inducible gene expression in Arabidopsis. , 2010, Molecular plant.

[11]  D. Job,et al.  Reboot the system thanks to protein post‐translational modifications and proteome diversity: How quiescent seeds restart their metabolism to prepare seedling establishment , 2011, Proteomics.

[12]  Control of the Phosphorylation State of the HPr Protein of the Phosphotransferase System in Bacillus subtilis: Implication of the Protein Phosphatase PrpC , 2007, Journal of Molecular Microbiology and Biotechnology.

[13]  Yu Xue,et al.  CPLM: a database of protein lysine modifications , 2013, Nucleic Acids Res..

[14]  Jay J Thelen,et al.  Modulation of Protein Phosphorylation, N-Glycosylation and Lys-Acetylation in Grape (Vitis vinifera) Mesocarp and Exocarp Owing to Lobesia botrana Infection* , 2012, Molecular & Cellular Proteomics.

[15]  A. Hershko,et al.  The ubiquitin system for protein degradation and some of its roles in the control of the cell division cycle* , 2005, Cell Death and Differentiation.

[16]  M. Mann,et al.  Lysine Acetylation Targets Protein Complexes and Co-Regulates Major Cellular Functions , 2009, Science.

[17]  P. Perata,et al.  Sugar uptake and transport in rice embryo. Expression of companion cell-specific sucrose transporter (OsSUT1) induced by sugar and light. , 2000, Plant physiology.

[18]  Dinshaw J. Patel,et al.  Multivalent engagement of chromatin modifications by linked binding modules , 2007, Nature Reviews Molecular Cell Biology.

[19]  Chunaram Choudhary,et al.  Proteome-Wide Mapping of the Drosophila Acetylome Demonstrates a High Degree of Conservation of Lysine Acetylation , 2011, Science Signaling.

[20]  Yi Zhang,et al.  The First Identification of Lysine Malonylation Substrates and Its Regulatory Enzyme* , 2011, Molecular & Cellular Proteomics.

[21]  D. Mount,et al.  Analysis of Histone Acetyltransferase and Histone Deacetylase Families of Arabidopsis Thaliana Suggests Functional Diversi®cation of Chromatin Modi®cation among Multicellular Eukaryotes , 2002 .

[22]  Ming Li,et al.  In-depth proteomic analysis of rice embryo reveals its important roles in seed germination. , 2014, Plant & cell physiology.

[23]  Nick V Grishin,et al.  Lysine Acetylation Is a Highly Abundant and Evolutionarily Conserved Modification in Escherichia Coli*S , 2009, Molecular & Cellular Proteomics.

[24]  T. Pawson,et al.  Post-translational modifications in signal integration , 2010, Nature Structural &Molecular Biology.

[25]  A. Millar,et al.  Ordered Assembly of Mitochondria During Rice Germination Begins with Promitochondrial Structures Rich in Components of the Protein Import Apparatus , 2005, Plant Molecular Biology.

[26]  Yingming Zhao,et al.  SIRT5-mediated lysine desuccinylation impacts diverse metabolic pathways. , 2013, Molecular cell.

[27]  Dorte B. Bekker-Jensen,et al.  Proteomic Analysis of Lysine Acetylation Sites in Rat Tissues Reveals Organ Specificity and Subcellular Patterns , 2012, Cell reports.

[28]  J. Thelen,et al.  Is Lys-Nɛ-acetylation the next big thing in post-translational modifications? , 2014, Trends in plant science.

[29]  B. Garcia,et al.  Tyr phosphorylation of PDP1 toggles recruitment between ACAT1 and SIRT3 to regulate the pyruvate dehydrogenase complex. , 2014, Molecular cell.

[30]  Hening Lin,et al.  Identification of Lysine Succinylation Substrates and the Succinylation Regulatory Enzyme CobB in Escherichia coli* , 2013, Molecular & Cellular Proteomics.

[31]  Frank Jordan,et al.  Inhibition of the Escherichia coli Pyruvate Dehydrogenase Complex E1 Subunit and Its Tyrosine 177 Variants by Thiamin 2-Thiazolone and Thiamin 2-Thiothiazolone Diphosphates , 2001, The Journal of Biological Chemistry.

[32]  Zhike Lu,et al.  Identification of 67 Histone Marks and Histone Lysine Crotonylation as a New Type of Histone Modification , 2011, Cell.

[33]  Jialing Yao,et al.  Constructing the metabolic and regulatory pathways in germinating rice seeds through proteomic approach , 2011, Proteomics.

[34]  Sebastian A. Wagner,et al.  Lysine succinylation is a frequently occurring modification in prokaryotes and eukaryotes and extensively overlaps with acetylation. , 2013, Cell reports.

[35]  Yixue Li,et al.  SysPTM: A Systematic Resource for Proteomic Research on Post-translational Modifications* , 2009, Molecular & Cellular Proteomics.

[36]  S. Liang,et al.  Systematic identification of the lysine lactylation in the protozoan parasite Toxoplasma gondii , 2014, Parasites & Vectors.

[37]  Pingfang Yang,et al.  Analysis of Proteome Profile in Germinating Soybean Seed, and Its Comparison with Rice Showing the Styles of Reserves Mobilization in Different Crops , 2013, PloS one.

[38]  Zhihong Zhang,et al.  Identification of lysine succinylation as a new post-translational modification. , 2011, Nature chemical biology.

[39]  J. Boeke,et al.  Lysine Succinylation and Lysine Malonylation in Histones* , 2012, Molecular & Cellular Proteomics.

[40]  A. Ismail,et al.  Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa). , 2009, Annals of botany.

[41]  Chunaram Choudhary,et al.  Proteome-wide Analysis of Lysine Acetylation Suggests its Broad Regulatory Scope in Saccharomyces cerevisiae* , 2012, Molecular & Cellular Proteomics.

[42]  Wei Liu,et al.  First succinyl-proteome profiling of extensively drug-resistant Mycobacterium tuberculosis revealed involvement of succinylation in cellular physiology. , 2015, Journal of proteome research.

[43]  Lei Pang,et al.  Proteome-wide lysine acetylation profiling of the human pathogen Mycobacterium tuberculosis. , 2015, The international journal of biochemistry & cell biology.

[44]  Pingfang Yang,et al.  Studies on the molecular mechanisms of seed germination , 2015, Proteomics.

[45]  Matthew J. Rardin,et al.  SIRT5 regulates the mitochondrial lysine succinylome and metabolic networks. , 2013, Cell metabolism.

[46]  P. Silver,et al.  Global histone acetylation induces functional genomic reorganization at mammalian nuclear pore complexes. , 2008, Genes & development.

[47]  L. Miguet,et al.  Proteins of Diverse Function and Subcellular Location Are Lysine Acetylated in Arabidopsis1[W][OA] , 2011, Plant Physiology.

[48]  B. Cravatt,et al.  Functional Lysine Modification by an Intrinsically Reactive Primary Glycolytic Metabolite , 2013, Science.

[49]  L. Noël,et al.  Role of SGT1 in resistance protein accumulation in plant immunity , 2006, The EMBO journal.

[50]  Mayandi Sivaguru,et al.  Lysine Acetylation Is a Widespread Protein Modification for Diverse Proteins in Arabidopsis1[C][W][OA] , 2011, Plant Physiology.

[51]  Zhongyi Cheng,et al.  Succinylome Analysis Reveals the Involvement of Lysine Succinylation in Metabolism in Pathogenic Mycobacterium tuberculosis* , 2015, Molecular & Cellular Proteomics.

[52]  A. Mirsky,et al.  ACETYLATION AND METHYLATION OF HISTONES AND THEIR POSSIBLE ROLE IN THE REGULATION OF RNA SYNTHESIS. , 1964, Proceedings of the National Academy of Sciences of the United States of America.

[53]  L. Tretter,et al.  Alpha-ketoglutarate dehydrogenase: a target and generator of oxidative stress , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[54]  Yi Tang,et al.  Lysine Propionylation and Butyrylation Are Novel Post-translational Modifications in Histones*S , 2007, Molecular & Cellular Proteomics.

[55]  Huadong Liu,et al.  Molecular Characterization of Propionyllysines in Non-histone Proteins *S , 2009, Molecular & Cellular Proteomics.

[56]  J. Thelen,et al.  Initial description of the developing soybean seed protein Lys-N(ε)-acetylome. , 2014, Journal of proteomics.

[57]  Pingfang Yang,et al.  Gene expression profile changes in germinating rice. , 2011, Journal of integrative plant biology.

[58]  S. Komatsu,et al.  Quantitative proteomics reveals the role of protein phosphorylation in rice embryos during early stages of germination. , 2014, Journal of proteome research.

引用
First Succinylome Profiling of Vibrio alginolyticus Reveals Key Role of Lysine Succinylation in Cellular Metabolism and Virulence
Frontiers in Cellular and Infection Microbiology
2021
Proteome-wide lysine acetylation identification in developing rice (Oryza sativa) seeds and protein co-modification by acetylation, succinylation, ubiquitination, and phosphorylation.
Biochimica et biophysica acta. Proteins and proteomics
2018
First Comprehensive Proteome Analyses of Lysine Acetylation and Succinylation in Seedling Leaves of Brachypodium distachyon L.
Scientific Reports
2016
Construction of a Quantitative Acetylomic Tissue Atlas in Rice (Oryza sativa L.)
Molecules
2018
Effects of PSII Manganese-Stabilizing Protein Succinylation on Photosynthesis in the Model Cyanobacterium Synechococcus sp. PCC 7002
Plant & cell physiology
2018
Large-Scale Assessment of Bioinformatics Tools for Lysine Succinylation Sites
Cells
2019
Proteome-wide Analysis of Lysine 2-hydroxyisobutyrylation in Developing Rice (Oryza sativa) Seeds
Scientific Reports
2017
Malonylome analysis in developing rice (Oryza sativa) seeds suggesting that protein lysine malonylation is well-conserved and overlaps with acetylation and succinylation substantially.
Journal of proteomics
2018
Proteomic analysis of lysine succinylation of the human pathogen Histoplasma capsulatum.
Journal of proteomics
2017
Lysine acetylome profiling uncovers novel histone deacetylase substrate proteins in Arabidopsis
Molecular systems biology
2017
Mapping the N-linked glycosites of rice (Oryza sativa L.) germinating embryos
PloS one
2017
Bringing New Methods to the Seed Proteomics Platform: Challenges and Perspectives
International journal of molecular sciences
2020
Lysine acetylation in mitochondria: From inventory to function.
Mitochondrion
2017
Global analysis of protein lysine succinylation profiles in common wheat
BMC Genomics
2017
Succinyl-proteome profiling of Dendrobium officinale, an important traditional Chinese orchid herb, revealed involvement of succinylation in the glycolysis pathway
BMC Genomics
2017
The first succinylome profile of Trichophyton rubrum reveals lysine succinylation on proteins involved in various key cellular processes
BMC Genomics
2017
Global Phosphoproteomic Analysis Reveals the Involvement of Phosphorylation in Aflatoxins Biosynthesis in the Pathogenic Fungus Aspergillus flavus
Scientific Reports
2016
Lysine Succinylation Contributes to Aflatoxin Production and Pathogenicity in Aspergillus flavus*
Molecular & Cellular Proteomics
2018
Malonylome Analysis Reveals the Involvement of Lysine Malonylation in Metabolism and Photosynthesis in Cyanobacteria.
Journal of proteome research
2017
Peroxiredoxins and Redox Signaling in Plants
Antioxidants & redox signaling
2017